Initiating a regenerative response; cellular and molecular features of wound healing in the cnidarian Nematostella vectensis

BMC Biology

Volumn 12, Issue 1, 2014, Pages

  DuBuc, Timothy Q ^a,b   Traylor Knowles, Nikki ^c   Martindale, Mark Q ^b  

^a UNIVERSITY OF HAWAII   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Cnidarians; ERK signaling; Gastrulation; Glycoprotein; Lateral gene transfer; Metalloproteinase; Microarray; Nematostella vectensis; Regeneration; Wound healing

Indexed keywords

CNIDARIA; NEMATOSTELLA VECTENSIS;

MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MUCIN; NOTCH RECEPTOR;

ANIMAL; APOPTOSIS; ARTICLE; BIOLOGICAL MODEL; CNIDARIA; CYTOLOGY; DNA MICROARRAY; DOWN REGULATION; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REGENERATION; SIGNAL TRANSDUCTION; TIME LAPSE IMAGING; UPREGULATION; WOUND HEALING;

ANIMALS; APOPTOSIS; CNIDARIA; DOWN-REGULATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; MAP KINASE SIGNALING SYSTEM; MODELS, BIOLOGICAL; MUCINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, NOTCH; REGENERATION; RNA, MESSENGER; TIME-LAPSE IMAGING; TRANSCRIPTION, GENETIC; UP-REGULATION; WOUND HEALING;

EID: 84907285121     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-12-24     Document Type: Article

References (88)

1. Gurtner GC, Werner S, Barrandon Y, Longaker MT. Wound repair and regeneration. Nature 2008, 453:314-321. 10.1038/nature07039, 18480812.
2. Brockes JP, Kumar A. Comparative aspects of animal regeneration. Annu Rev Cell Dev Biol 2008, 24:525-549. 10.1146/annurev.cellbio.24.110707.175336, 18598212.
3. Mescher AL. Effects on adult newt limb regeneration of partial and complete skin flaps over the amputation surface. J Exp Zool 1976, 195:117-128. 10.1002/jez.1401950111, 1255117.
4. Newman SA. The interaction of the organizing regions in Hydra and its possible relation to the role of the cut end in regeneration. J Embryol Exp Morphol 1974, 31:541-555.
5. Silver J, Miller JH. Regeneration beyond the glial scar. Nat Rev Neurosci 2004, 5:146-156. 10.1038/nrn1326, 14735117.
6. Hyman LH. The Invertebrates: Protozoa through Ctenophora 1940, New York: McGraw Hill.
7. Matus DQ, Pang K, Marlow H, Dunn CW, Thomsen GH, Martindale MQ. Molecular evidence for deep evolutionary roots of bilaterality in animal development. Proc Natl Acad Sci USA 2006, 103:11195-11200. 10.1073/pnas.0601257103, 1544064, 16837574.
8. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, Jurka J, Genikhovich G, Grigoriev IV, Lucas SM, Steele RE, Finnerty JR, Technau U, Martindale MQ, Rokhsar DS. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 2007, 317:86-94. 10.1126/science.1139158, 17615350.
9. Saina M, Genikhovich G, Renfer E, Technau U. BMPs and chordin regulate patterning of the directive axis in a sea anemone. Proc Natl Acad Sci USA 2009, 106:18592-18597. 10.1073/pnas.0900151106, 2773963, 19833871.
10. Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Quéinnec E, Da Silva C, Wincker P, Le Guyader H, Leys S, Jackson DJ, Schreiber F, Erpenbeck D, Morgenstern B, Wörheide G, Manuel M. Phylogenomics revives traditional views on deep animal relationships. Curr Biol 2009, 19:706-712. 10.1016/j.cub.2009.02.052, 19345102.
11. Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguñà J, Bailly X, Jondelius U, Wiens M, Müller WEG, Seaver E, Wheeler WC, Martindale MQ, Giribet G, Dunn CW. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc Biol Sci 2009, 276:4261-4270. 10.1098/rspb.2009.0896, 2817096, 19759036.
12. Holstein TW, Hobmayer E, Technau U. Cnidarians: an evolutionarily conserved model system for regeneration?. Dev Dyn 2003, 226:257-267. 10.1002/dvdy.10227, 12557204.
13. Reitzel AM, Burton PM, Krone C, Finnerty JR. Comparison of developmental trajectories in the starlet sea anemone Nematostella vectensis: embryogenesis, regeneration, and two forms of asexual fission. Invertebr Biol 2007, 126:99-112.
14. Tucker RP, Shibata B, Blankenship TN. Ultrastructure of the mesoglea of the sea anemone Nematostella vectensis (Edwardsiidae). Invertebr Biol 2011, 130:11-24.
15. Trevino M, Stefanik DJ, Rodriguez R, Harmon S, Burton PM. Induction of canonical Wnt signaling by alsterpaullone is sufficient for oral tissue fate during regeneration and embryogenesis in Nematostella vectensis. Dev Dyn 2011, 240:2673-2679. 10.1002/dvdy.22774, 3672222, 22052821.
16. Passamaneck YJ, Martindale MQ. Cell proliferation is necessary for the regeneration of oral structures in the anthozoan cnidarian Nematostella vectensis. BMC Dev Biol 2012, 12:34. 10.1186/1471-213X-12-34, 3553063, 23206430.
17. Stefanik DJ, Friedman LE, Finnerty JR. Collecting, rearing, spawning and inducing regeneration of the starlet sea anemone, Nematostella vectensis. Nat Protoc 2013, 8:916-923. 10.1038/nprot.2013.044, 23579780.
18. Bossert PE, Dunn MP, Thomsen GH. A staging system for the regeneration of a polyp from the aboral physa of the anthozoan cnidarian Nematostella vectensis. Dev Dyn 2013, 242:1320-1331. 10.1002/dvdy.24021, 23913838.
19. Holstein TW, Hobmayer E, David CN. Pattern of epithelial cell cycling in Hydra. Dev Biol 1991, 148:602-611. 10.1016/0012-1606(91)90277-A, 1743403.
20. Park H, Ortmeyer A, Blankenbaker D. Cell division during regeneration in Hydra. Nature 1970, 227:617-619. 10.1038/227617a0, 4393366.
21. Reitzel AM, Sullivan JC, Traylor-Knowles N, Finnerty JR. Genomic survey of candidate stress-response genes in the estuarine anemone Nematostella vectensis. Biol Bull 2008, 214:233-254. 10.2307/25470666, 18574101.
22. Wang S, Tsarouhas V, Xylourgidis N, Sabri N, Tiklová K, Nautiyal N, Gallio M, Samakovlis C. The tyrosine kinase Stitcher activates Grainy head and epidermal wound healing in Drosophila. Nat Cell Biol 2009, 11:890-895. 10.1038/ncb1898, 19525935.
23. Matsubayashi Y, Ebisuya M, Honjoh S, Nishida E. ERK activation propagates in epithelial cell sheets and regulates their migration during wound healing. Curr Biol 2004, 14:731-735.
24. Kim M, McGinnis W. Phosphorylation of Grainy head by ERK is essential for wound-dependent regeneration but not for development of an epidermal barrier. Proc Natl Acad Sci USA 2011, 108:650-655. 10.1073/pnas.1016386108, 3021071, 21187384.
25. Surachetpong W, Singh N, Cheung KW, Luckhart S. MAPK ERK signaling regulates the TGF-beta1-dependent mosquito response to Plasmodium falciparum. PLoS Pathog 2009, 5:e1000366. 10.1371/journal.ppat.1000366, 2658807, 19343212.
26. Furler RL, Uittenbogaart CH. Signaling through the P38 and ERK pathways: a common link between HIV replication and the immune response. Immunol Res 2010, 48:99-109. 10.1007/s12026-010-8170-1, 20725863.
27. Odendall C, Rolhion N, Förster A, Poh J, Lamont DJ, Liu M, Freemont PS, Catling AD, Holden DW. The Salmonella kinase SteC targets the MAP kinase MEK to regulate the host actin cytoskeleton. Cell Host Microbe 2012, 12:657-668. 10.1016/j.chom.2012.09.011, 3510437, 23159055.
28. Renfer E, Amon-Hassenzahl A, Steinmetz PRH, Technau U. A muscle-specific transgenic reporter line of the sea anemone, Nematostella vectensis. Proc Natl Acad Sci USA 2010, 107:104-108. 10.1073/pnas.0909148107, 2806778, 20018670.
29. Chera S, Ghila L, Dobretz K, Wenger Y, Bauer C, Buzgariu W, Martinou J-C, Galliot B. Apoptotic cells provide an unexpected source of Wnt3 signaling to drive Hydra head regeneration. Dev Cell 2009, 17:279-289. 10.1016/j.devcel.2009.07.014, 19686688.
30. Bergmann A, Steller H. Apoptosis, stem cells, and tissue regeneration. Sci Signal 2010, 3:re8. 2991142, 20978240.
31. Penn JW, Grobbelaar AO, Rolfe KJ. The role of the TGF-β family in wound healing, burns and scarring: a review. Int J Burns Trauma 2012, 2:18-28. 3415964, 22928164.
32. Genome of Nematostella vectensis. [http://genome.jgi-psf.org/Nemve1/Nemve1.home.html].
33. Wikramanayake AH, Hong M, Lee PN, Pang K, Byrum CA, Bince JM, Xu R, Martindale MQ. An ancient role for nuclear beta-catenin in the evolution of axial polarity and germ layer segregation. Nature 2003, 426:446-450. 10.1038/nature02113, 14647383.
34. Martindale MQ, Pang K, Finnerty JR. Investigating the origins of triploblasty: " mesodermal" gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 2004, 131:2463-2474. 10.1242/dev.01119, 15128674.
35. Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev 2003, 83:835-870.
36. Gill SE, Parks WC. Metalloproteinases and their inhibitors: regulators of wound healing. Int J Biochem Cell Biol 2008, 40:1334-1347. 10.1016/j.biocel.2007.10.024, 2746915, 18083622.
37. Montagnani C, Le Roux F, Berthe F, Escoubas JM. Cg-TIMP, an inducible tissue inhibitor of metalloproteinase from the Pacific oyster Crassostrea gigas with a potential role in wound healing and defense mechanisms (1). FEBS Lett 2001, 500:64-70. 10.1016/S0014-5793(01)02559-5, 11434928.
38. Mott JD, Werb Z. Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol 2004, 16:558-564. 10.1016/j.ceb.2004.07.010, 2775446, 15363807.
39. Shimizu H, Zhang X, Zhang J, Leontovich A, Fei K, Yan L, Sarras MP. Epithelial morphogenesis in Hydra requires de novo expression of extracellular matrix components and matrix metalloproteinases. Development 2002, 129:1521-1532.
40. Altincicek B, Vilcinskas A. Comparative analysis of septic injury-inducible genes in phylogenetically distant model organisms of regeneration and stem cell research, the planarian Schmidtea mediterranea and the cnidarian Hydra vulgaris. Front Zool 2008, 5:6. 10.1186/1742-9994-5-6, 2386466, 18439314.
41. Campbell LJ, Suárez-Castillo EC, Ortiz-Zuazaga H, Knapp D, Tanaka EM, Crews CM. Gene expression profile of the regeneration epithelium during axolotl limb regeneration. Dev Dyn 1826-1840, 2011:240.
42. Cooper L, Johnson C, Burslem F, Martin P. Wound healing and inflammation genes revealed by array analysis of " macrophageless" PU.1 null mice. Genome Biol 2005, 6:R5. 10.1186/gb-2005-6-4-p5, 549066, 15642097.
43. Cole J, Tsou R, Wallace K, Gibran N, Isik F. Early gene expression profile of human skin to injury using high-density cDNA microarrays. Wound Repair Regen 2001, 9:360-370. 10.1046/j.1524-475x.2001.00360.x, 11896979.
44. Harland B, Walcott S, Sun SX. Adhesion dynamics and durotaxis in migrating cells. Phys Biol 2011, 8:015011. 10.1088/1478-3975/8/1/015011, 21301061.
45. Plotnikov SV, Waterman CM. Guiding cell migration by tugging. Curr Opin Cell Biol 2013, 25:619-626. 10.1016/j.ceb.2013.06.003, 23830911.
46. Fabila Y, Navarro L, Fujisawa T, Bode HR, Salgado LM. Selective inhibition of protein kinases blocks the formation of a new axis, the beginning of budding, in Hydra. Mech Dev 2002, 119:157-164. 10.1016/S0925-4773(02)00351-9, 12464429.
47. Manuel GC, Reynoso R, Gee L, Salgado LM, Bode HR. PI3K and ERK 1-2 regulate early stages during head regeneration in Hydra. Dev Growth Differ 2006, 48:129-138. 10.1111/j.1440-169X.2006.00847.x, 16512856.
48. Chera S, Ghila L, Wenger Y, Galliot B. Injury-induced activation of the MAPK/CREB pathway triggers apoptosis-induced compensatory proliferation in hydra head regeneration. Dev Growth Differ 2011, 53:186-201. 10.1111/j.1440-169X.2011.01250.x, 21338345.
49. Tasaki J, Shibata N, Nishimura O, Itomi K, Tabata Y, Son F, Suzuki N, Araki R, Abe M, Agata K, Umesono Y. ERK signaling controls blastema cell differentiation during planarian regeneration. Development 2011, 138:2417-2427. 10.1242/dev.060764, 21610023.
50. Münder S, Käsbauer T, Prexl A, Aufschnaiter R, Zhang X, Towb P, Böttger A. Notch signalling defines critical boundary during budding in Hydra. Dev Biol 2010, 344:331-345. 10.1016/j.ydbio.2010.05.517, 20534380.
51. Marlow H, Roettinger E, Boekhout M, Martindale MQ. Functional roles of Notch signaling in the cnidarian Nematostella vectensis. Dev Biol 2012, 362:295-308. 10.1016/j.ydbio.2011.11.012, 3771581, 22155407.
52. Lang T, Hansson GC, Samuelsson T. Gel-forming mucins appeared early in metazoan evolution. Proc Natl Acad Sci USA 2007, 104:16209-16214. 10.1073/pnas.0705984104, 2042186, 17911254.
53. Ikezawa T, Goso Y, Ichikawa T, Hayashida H, Kurihara M, Okayasu I, Saigenji K, Ishihara K. Appearance of specific mucins recognized by monoclonal antibodies in rat gastric mucosa healing from HCl-induced gastric mucosal damage. J Gastroenterol 2004, 39:113-119. 10.1007/s00535-003-1261-1, 15069617.
54. Wallace JL, Vong L, Dharmani P, Srivastava V, Chadee K. Muc-2-deficient mice display a sex-specific, COX-2-related impairment of gastric mucosal repair. Am J Pathol 2011, 178:1126-1133. 10.1016/j.ajpath.2010.11.048, 3069899, 21356364.
55. Ho SB, Dvorak LA, Moor RE, Jacobson AC, Frey MR, Corredor J, Polk DB, Shekels LL. Cysteine-rich domains of muc3 intestinal mucin promote cell migration, inhibit apoptosis, and accelerate wound healing. Gastroenterology 2006, 131:1501-1517. 10.1053/j.gastro.2006.09.006, 17101324.
56. Tran C, Hadfield M. Larvae of Pocillopora damicornis (Anthozoa) settle and metamorphose in response to surface-biofilm bacteria. Mar Ecol Prog Ser 2011, 433:85-96.
57. Devuyst O, Dahan K, Pirson Y. Tamm-Horsfall protein or uromodulin: new ideas about an old molecule. Nephrol Dial Transplant 2005, 20:1290-1294. 10.1093/ndt/gfh851, 15840660.
58. El-Achkar TM, McCracken R, Liu Y, Heitmeier MR, Bourgeois S, Ryerse J, Wu X-R. Tamm-Horsfall protein translocates to the basolateral domain of thick ascending limbs, interstitium, and circulation during recovery from acute kidney injury. Am J Physiol Renal Physiol 2013, 304:F1066-F1075. 10.1152/ajprenal.00543.2012, 3625838, 23389456.
59. Bibb C, Campbell RD. Tissue healing and septate desmosome formation in Hydra. Tissue Cell 1973, 5:23-35. 10.1016/S0040-8166(73)80003-5, 4693989.
60. Magie CR, Pang K, Martindale MQ. Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis. Dev Genes Evol 2005, 215:618-630. 10.1007/s00427-005-0022-y, 16193320.
61. Shinzato C, Iguchi A, Hayward DC, Technau U, Ball EE, Miller DJ. Sox genes in the coral Acropora millepora: divergent expression patterns reflect differences in developmental mechanisms within the Anthozoa. BMC Evol Biol 2008, 8:311. 10.1186/1471-2148-8-311, 2613919, 19014479.
62. Lee Y-H, Aoki Y, Hong C-S, Saint-Germain N, Credidio C, Saint-Jeannet J-P. Early requirement of the transcriptional activator Sox9 for neural crest specification in Xenopus. Dev Biol 2004, 275:93-103. 10.1016/j.ydbio.2004.07.036, 15464575.
63. Sakai D, Suzuki T, Osumi N, Wakamatsu Y. Cooperative action of Sox9, Snail2 and PKA signaling in early neural crest development. Development 2006, 133:1323-1333. 10.1242/dev.02297, 16510505.
64. Mardaryev AN, Meier N, Poterlowicz K, Sharov AA, Sharova TY, Ahmed MI, Rapisarda V, Lewis C, Fessing MY, Ruenger TM, Bhawan J, Werner S, Paus R, Botchkarev VA. Lhx2 differentially regulates Sox9, Tcf4 and Lgr5 in hair follicle stem cells to promote epidermal regeneration after injury. Development 2011, 138:4843-4852. 10.1242/dev.070284, 22028024.
65. Magie CR, Daly M, Martindale MQ. Gastrulation in the cnidarian Nematostella vectensis occurs via invagination not ingression. Dev Biol 2007, 305:483-497. 10.1016/j.ydbio.2007.02.044, 17397821.
66. Brown KL, Phillips TJ. Nutrition and wound healing. Clin Dermatol 2010, 28:432-439. 10.1016/j.clindermatol.2010.03.028, 20620761.
67. Margadant C, Charafeddine RA, Sonnenberg A. Unique and redundant functions of integrins in the epidermis. FASEB J 2010, 24:4133-4152. 10.1096/fj.09-151449, 20624931.
68. Knack BA, Iguchi A, Shinzato C, Hayward DC, Ball EE, Miller DJ. Unexpected diversity of cnidarian integrins: expression during coral gastrulation. BMC Evol Biol 2008, 8:136. 10.1186/1471-2148-8-136, 2397394, 18466626.
69. Becchetti A, Arcangeli A. Integrins and ion channels in cell migration: implications for neuronal development, wound healing and metastatic spread. Adv Exp Med Biol 2010, 674:107-123. 10.1007/978-1-4419-6066-5_10, 20549944.
70. Reyes-Bermudez A, Desalvo MK, Voolstra CR, Sunagawa S, Szmant AM, Iglesias-Prieto R, Medina M. Gene expression microarray analysis encompassing metamorphosis and the onset of calcification in the scleractinian coral Montastraea faveolata. Mar Genomics 2009, 2:149-159. 10.1016/j.margen.2009.07.002, 21798184.
71. Goh Then Sin C, Hersch N, Rudland PS, Barraclough R, Hoffmann B, Gross SR. S100A4 downregulates filopodia formation through increased dynamic instability. Cell Adh Migr 2011, 5:439-447. 10.4161/cam.5.5.17773, 3218611, 21975553.
72. Rentzsch F, Fritzenwanker JH, Scholz CB, Technau U. FGF signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis. Development 2008, 135:1761-1769. 10.1242/dev.020784, 18441276.
73. Matus DQ, Thomsen GH, Martindale MQ. FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian. Dev Genes Evol 2007, 217:137-148. 10.1007/s00427-006-0122-3, 17237944.
74. Sinigaglia C, Busengdal H, Leclère L, Technau U, Rentzsch F. The bilaterian head patterning gene six3/6 controls aborald development in a cnidarian. PLoS Biol 2013, 11:e1001488. 10.1371/journal.pbio.1001488, 3586664, 23483856.
75. Arvizu F, Aguilera A, Salgado LM. Activities of the protein kinases STK, PI3K, MEK, and ERK are required for the development of the head organizer in Hydra magnipapillata. Differentiation 2006, 74:305-312. 10.1111/j.1432-0436.2006.00078.x, 16831199.
76. Hand C, Uhlinger KR. The unique, widely distributed, estuarine sea anemone, Nematostella vectensis Stephenson: a review, new facts, and questions. Estuaries 1994, 17:501-508.
77. Cohen M, Varki NM, Jankowski MD, Gagneux P. Using unfixed, frozen tissues to study natural mucin distribution. J Vis Exp 2012, 67:e3928. 3490269, 23023050.
78. Volocity 3D Image Analysis Software. [http://www.improvision.com].
79. Layden MJ, Boekhout M, Martindale MQ. Nematostella vectensis achaete-scute homolog NvashA regulates embryonic ectodermal neurogenesis and represents an ancient component of the metazoan neural specification pathway. Development 2012, 139:1013-1022. 10.1242/dev.073221, 3274362, 22318631.
80. Röttinger E, Dahlin P, Martindale MQ. A framework for the establishment of a cnidarian gene regulatory network for " endomesoderm" specification: the inputs of ß-catenin/TCF signaling. PLoS Genet 2012, 8:e1003164. 10.1371/journal.pgen.1003164, 3531958, 23300467.
81. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003, 19:185-193. 10.1093/bioinformatics/19.2.185, 12538238.
82. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264. 10.1093/biostatistics/4.2.249, 12925520.
83. ArrayExpress, functional genomics data. [https://www.ebi.ac.uk/arrayexpress/].
84. Basic Local Alignment Search Tool. [http://blast.ncbi.nlm.nih.gov].
85. Blast2Go. [http://www.blast2go.com/b2ghome].
86. MacVector Alignment Software. [http://www.macvector.com].
87. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
88. Pang K, Matus DQ, Martindale MQ. The ancestral role of COE genes may have been in chemoreception: evidence from the development of the sea anemone, Nematostella vectensis (Phylum Cnidaria; Class Anthozoa). Dev Genes Evol 2004, 214:134-138. 10.1007/s00427-004-0383-7, 14752662.